Optional strategies for reduced metabolism in gray mouse lemurs.

Among the order of primates, torpor has been described only for the small Malagasy cheirogaleids Microcebus and Cheirogaleus. The nocturnal, gray mouse lemur, Microcebus murinus (approx. 60 g), is capable of entering into and spontaneously arousing from apparently daily torpor during the dry season in response to reduced temperatures and low food and water sources. Mark-recapture studies indicated that this primate species might also hibernate for several weeks, although physiological evidence is lacking. In the present study, we investigated patterns of body temperature in two free-ranging M. murinus during the austral winter using temperature-sensitive data loggers implanted subdermally. One lemur hibernated and remained inactive for 4 weeks. During this time, body temperature followed the ambient temperature passively with a minimum body temperature of 11.5 degrees C, interrupted by irregular arousals to normothermic levels. Under the same conditions, the second individual displayed only short bouts of torpor in the early morning hours but maintained stable normothermic body temperatures throughout its nocturnal activity. Reduction of body temperature was less pronounced in the mouse lemur that utilized short bouts of torpor with a minimum value of 27 degrees C. Despite the small sample size, our findings provide the first physiological confirmation that free-ranging individuals of M. murinus from the humid evergreen littoral rain forest have the option to utilize short torpor bouts or hibernation under the same conditions as two alternative energy-conserving physiological solutions to environmental constraints.

Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar.

Hybrid zones in ecotones can be useful model systems for the study of evolutionary processes that shape the distribution and discreteness of species. Such studies could be important for an improved understanding of the complex biogeography of Madagascar, which is renowned for its outstanding degree of small-scale endemism. Certain forest remnants in central Madagascar indicate that transitional corridors across the island could have connected microendemics in different forest types in the past. Evolutionary processes in such corridors are difficult to study because most of these corridors have disappeared due to deforestation in central Madagascar. We studied a hybrid zone in one of the few remaining ecotonal corridors between dry and humid forests in Madagascar, which connects two species of mouse lemurs, Microcebus griseorufus in dry spiny forest and Microcebus murinus in humid littoral forest. We sampled 162 mouse lemurs at nine sites across this boundary. Morphometric analyses revealed intermediate morphotypes of many individuals in transitional habitat. Bayesian clustering of microsatellite genotypes and assignment tests yielded evidence for a mixed ancestry of mouse lemurs in the ecotone, where we also observed significant linkage disequilibria and heterozygote deficiency. In contrast to these observations, mitochondrial haplotypes displayed a sharply delimited boundary at the eastern edge of spiny forest, which was noncoincident with the signals from microsatellite data. Among several alternative scenarios, we propose asymmetric nuclear introgression due to male-biased dispersal, divergent environmental selection, and an expansion of dry spiny forest in the course of aridification as a probable explanation of our observations.

Improved recruitment of a lemur-dispersed tree in Malagasy dry forests after the demise of vertebrates in forest fragments.

The objective of this study was to examine how the processes of seed dispersal and seed predation were altered in forest fragments of the dry forest of Madagascar, where the usual seed dispersers and vertebrate seed predators were absent, using a lemur-dispersed tree species (Strychnos madagascariensis; Loganiaceae) as an example. We then assessed how the changes in vertebrate community composition alter the regeneration pattern and establishment of this tree species and thus, ultimately, the species composition of the forest fragments. By using size-selective exclosures, data from forest fragments were compared with results from continuous forest where vertebrate dispersers and predators were abundant. Visits to the exclosures by mammalian seed predators were monitored with hair traps. In the continuous forest up to 100% of the seeds were removed within the 7 days of the experiments. A substantial proportion of them was lost to seed predation by native rodents. In contrast, practically no predation took place in the forest fragments and almost all seeds removed were dispersed into the safety of ant nests by Aphaenogaster swammerdami, which improves chances of seedling establishment. In congruence with these findings, the abundance of S. madagascariensis in the forest fragments exceeded that of the continuous forest. Thus, the lack of vertebrate seed dispersers in these forest fragments did not lead to a decline in regeneration of this animal-dispersed tree species as would have been expected, but rather was counterbalanced by the concomitant demise of vertebrate seed predators and an increased activity of ants taking over the role of seed dispersers, and possibly even out-doing the original candidates. This study provides an example of a native vertebrate-dispersed species apparently profiting from fragmentation due to flexible animal-plant interactions in different facets, possibly resulting in an impoverished tree species community.

Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus.

We investigated the importance of the major histocompatibility complex (MHC) constitution on the parasite burden of free-ranging mouse lemurs (Microcebus murinus) in four littoral forest fragments in southeastern Madagascar. Fourteen different MHC class II DRB-exon 2 alleles were found in 228 individuals with high levels of sequence divergence between alleles. More nonsynonymous than synonymous substitutions in the functional important antigen recognition and binding sites indicated selection processes maintaining MHC polymorphism. Animals from the four forest fragments differed in their infection status (being infected or not), in the number of different nematode morphotypes per individual (NNI) as well as in the fecal egg counts (FEC) values. Heterozygosity in general was uncorrelated with any of these measures of infection. However, a positive relationship was found between specific alleles and parasite load. Whereas the common allele Mimu-DRB*1 was more frequently found in infected individuals and in individuals with high NNI and FEC values (high parasite load), the rare alleles Mimu-DRB*6 and 10 were more prevalent in uninfected individuals and in individuals with low NNI and FEC values (low parasite load). These three alleles associated with parasite load had unique amino acid motifs in the antigen binding sites. This distinguished them from the remaining 11 Mimu-DRB alleles. Our results support the hypothesis that MHC polymorphism in M. murinus is maintained through pathogen-driven selection acting by frequency-dependent selection. This is the first study of the association of MHC variation and parasite burden in a free-ranging primate.

A comparison of morphological and chemical fruit traits between two sites with different frugivore assemblages.

Large-scale comparisons might reveal matching between fruit traits and frugivore assemblages that might be cryptic on a local scale. Therefore, we compared morphological (colour, size, husk thickness) and chemical fruit traits (protein, nitrogen, sugar, lipid, tannin and fibre content) between Malagasy and South African tree communities with different frugivore communities. In Madagascar, where lemurs are important seed dispersers, we found more tree species with fruit colour classified as "primate fruits". In contrast, in South Africa we found more tree species with fruits classified as "bird coloured". This correlated with the greater importance of frugivorous birds in South Africa vs. Madagascar. Additionally, we found higher sugar concentrations in fruits from the South African tree community and higher fibre content in fruits from the Malagasy tree community. However, fibre content could be related to differences in abiotic conditions between the two study sites. This suggests that fruit colour more than other morphological and chemical fruit traits, reflects food selection by the different frugivore assemblages of those two sites.

White adipose tissue composition in the free-ranging fat-tailed dwarf lemur (Cheirogaleus medius; Primates), a tropical hibernator.

In temperate species, hibernation is enhanced by high levels of essential fatty acids in white adipose tissue. Essential fatty acids cannot be synthesized by mammals, thus nutritional ecology should play a key role in physiological adaptations to hibernation. Tropical hibernators are exposed to different physiological demands than hibernators in temperate regions and are expected to be subject to different constraints. The aims of this study were to assess whether or not the tropical hibernator Cheirogaleus medius shows biochemical changes in its white adipose tissue before and during hibernation. A capture-recapture study was combined with feeding observations in western Madagascar. Before and after hibernation, 77 samples of white adipose tissue from 57 individuals of C. medius, as well as dietary items eaten during pre-hibernation fattening, were sampled and analyzed for their fatty acid composition. In contrast to temperate hibernators, C. medius exhibits extremely low essential fatty acid concentrations in its white adipose tissue (2.5%) prior to hibernation. The fatty acid pattern of the white adipose tissue did not change during pre-hibernation fattening and did not reflect dietary fatty acid composition. During hibernation, fat stores showed only minor but significant compositional changes. Because of its prevalence, the main fuel during hibernation was the monounsaturated oleic acid, which seemed to be preferentially synthesized from dietary carbohydrates. Results suggest that essential fatty acids do not represent an ecological limitation for hibernation in the tropics, at least not in the fat-tailed dwarf lemur.

Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus).

Phylogenetic analysis of mtDNA sequence data confirms the observation that species diversity in the world's smallest living primate (genus Microcebus) has been greatly underestimated. The description of three species new to science, and the resurrection of two others from synonymy, has been justified on morphological grounds and is supported by evidence of reproductive isolation in sympatry. This taxonomic revision doubles the number of recognized mouse lemur species. The molecular data and phylogenetic analyses presented here verify the revision and add a historical framework for understanding mouse lemur species diversity. Phylogenetic analysis revises established hypotheses of ecogeographic constraint for the maintenance of species boundaries in these endemic Malagasy primates. Mouse lemur clades also show conspicuous patterns of regional endemism, thereby emphasizing the threat of local deforestation to Madagascar's unique biodiversity.

[Lemurs of Madagascar. Tests on evolution of primate communities]. / Lemuren Madagaskars. Tests zur Evolution von Primatengemeinschaften.

The flora and fauna of Madagascar evolved rather independently from the African mainland. In contrast to other oceanic islands, Madagascar is large enough to house most major components of tropical ecosystems, allowing tests of evolutionary hypotheses on the level of complete communities. Taking lemurs, the primates of Madagascar, as an example, evolutionary hypotheses correctly predict the organization of their community structure with respect to ecological correlates. Lemur social systems and their morphological correlates, on the other hand, deviate largely from the typical mammalian pattern. Thus, the traditional hypotheses of behavioral ecology, based solely on resource distribution and predation pressure, are insufficient to explain the existing variability in lemur social systems. Other factors, such as activity patterns and avoidance of infanticide, may be equally important. Due to interspecific variation in these characters, lemurs offer the unique opportunity to determine the relative importance of these factors for the evolution of social systems.

Orientation in birds. The sun compass.

The sun compass was discovered by G. Kramer in caged birds showing migratory restlessness. Subsequent experiments with caged birds employing directional training and clock shifts, carried out by Hoffman and Schmidt-Koenig, showed that the sun azimuth is used, and the sun altitude ignored. In the laboratory, McDonald found the accuracy to be +/- 3 degrees(-)+/- 5 degrees. According to Hoffmann and Schmidt-Koenig, caged birds trained at medium northern latitudes were able to allow for the sun's apparent movement north of the arctic circle, but not in equatorial and trans-equatorial latitudes. In homing experiments, and employing clock shifts, Schmidt-Koenig demonstrated that the sun compass is used by homing pigeons during initial orientation. This finding is the principal evidence for the existence of a map-and-compass navigational system. Pigeons living in equatorial latitudes utilize the sun compass even under the extreme solar conditions of equinox, achieving angular resolution of about 3 degrees in homing experiments. According to preliminary analyses, the homing pigeons' ephemerides are retarded by several weeks (Ranvaud, Schmidt-Koenig, Ganzhorn et al.).

Seasonal variation in the orientation of homing pigeons: new evidence for a latency in the sun compass.

Homing pigeons must keep track of the seasonal variations in the sun's daily motion to use the sun as a reference. A delay of seven weeks in such updating of their ephemerides was previously interpreted as being the cause of the behavior of control pigeons studied near the equator in September, when birds released in the morning flew anomalously to the right of birds released in the afternoon. Demonstration of the chronic existence of a delay was obtained by observing that the anomaly was still present but inverted in sign in March, when the pigeons released in the morning flew to the left of those released in the afternoon.

Seasonal variation in the orientation of homing pigeons: new evidence for a latency in the sun compass

Homing pigeons must keep track of the seasonal variations in the sun's daily motion to use the sun as a reference. A delay of seven weeks in such updating of their ephemerides was previously interpreted as being the cause of the behavior of control pigeons studied near the equator in September, when birds released in the morning flew anomalously to the right of birds released in the afternoon. Demonstration of the chronic existence of a delay was obtained by observing that the anomaly was still present but inverted in sign in March, when the pigeons released in the morning flew to the left of those released in the afternoon

The impact of selective logging on forest structure and tenrec populations in western Madagascar.

This paper reports on possible effects of selective logging on vegetation structure and its consequences for two tenrec species in a dry forest in western Madagascar. On a small scale semi-mechanized logging of less than 10 m3 per ha alters forest structure significantly. However on a large scale most of these changes are smaller than the variation of forest structure due to natural causes. The most profound ecological effect of logging is a reduction in the number of woody species in the regenerating cohort of trees. Potential longterm consequences of this feature are discussed. Microhabitat variables influencing the habitat utilization of two tenrec species,Echinops telfairi andTenrec ecaudatus, were identified in an area of unlogged forest. The conclusions derived from this analysis were then tested in other parts of the forest which had been modified by selective logging. Logging of the extent described above slightly impairs habitats forE. telfairi but has no effect onT. ecaudatus. Though the latter species is hunted extensively in the logged areas, loggingper se does not threaten the survival of either species.

The aye-aye (Daubentonia madagascariensis) found in the eastern rainforest of Madagascar.

In the course of a study on the ecology of nocturnal lemurs several aye-aye (Daubentonia madagascariensis) were seen in the eastern rainforest of Madagascar near Perinet. These observations of the aye-aye in a forest of higher altitude suggest a still much wider distribution of this species than previously thought.

Habitat separation of semifree-ranging Lemur catta and Lemur fulvus.

Habitat use of two semifree-ranging groups of lemurs, Lemur catta and Lemur fulvus, was studied in relation to abiotic, floristic, and structural characteristics of their enclosure. L. catta was very flexible in the use of the habitat and showed a tendency for random utilization. But this species reacted quickly to changes of the abiotic environment. L. fulvus preferred to stay in areas with dense vegetation but good lateral visibility and close to the food plants. Abiotic factors such as solar radiation and ambient temperature influenced L. fulvus to a lesser extent than L. catta. According to these results L. catta could be considered to be adapted to variable environments where it is advantageous to react quickly to changes of abiotic factors. The conservative habitat use and the limited response to abiotic factors of L. fulvus might reflect adaptations of a species living in a stable environment. If these interpretations prove correct, then this study provides another example of animals born and raised in captivity that have retained habitat preferences of their wild conspecifics.